The E3 ubiquitin ligase Sina regulates the assembly and disassembly of the synaptonemal complex in Drosophila females

PLoS Genet. 2019 May 20;15(5):e1008161. doi: 10.1371/journal.pgen.1008161. eCollection 2019 May.

Abstract

During early meiotic prophase, homologous chromosomes are connected along their entire lengths by a proteinaceous tripartite structure known as the synaptonemal complex (SC). Although the components that comprise the SC are predominantly studied in this canonical ribbon-like structure, they can also polymerize into repeated structures known as polycomplexes. We find that in Drosophila oocytes, the ability of SC components to assemble into canonical tripartite SC requires the E3 ubiquitin ligase Seven in absentia (Sina). In sina mutant oocytes, SC components assemble into large rod-like polycomplexes instead of proper SC. Thus, the wild-type Sina protein inhibits the polymerization of SC components, including those of the lateral element, into polycomplexes. These polycomplexes persist into meiotic stages when canonical SC has been disassembled, indicating that Sina also plays a role in controlling SC disassembly. Polycomplexes induced by loss-of-function sina mutations associate with centromeres, sites of double-strand breaks, and cohesins. Perhaps as a consequence of these associations, centromere clustering is defective and crossing over is reduced. These results suggest that while features of the polycomplexes can be recognized as SC by other components of the meiotic nucleus, polycomplexes nonetheless fail to execute core functions of canonical SC.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Cycle Proteins / metabolism
  • Cell Nucleus / metabolism
  • Centromere / metabolism
  • Chromosomal Proteins, Non-Histone / metabolism
  • Chromosome Pairing / genetics
  • Cohesins
  • Cytoskeletal Proteins / genetics
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / genetics
  • Female
  • Meiosis
  • Nuclear Proteins / metabolism*
  • Nuclear Proteins / physiology*
  • Oocytes / metabolism
  • Synaptonemal Complex / genetics
  • Synaptonemal Complex / metabolism*
  • Ubiquitin-Protein Ligases / metabolism*
  • Ubiquitin-Protein Ligases / physiology*

Substances

  • Cell Cycle Proteins
  • Chromosomal Proteins, Non-Histone
  • Cytoskeletal Proteins
  • Drosophila Proteins
  • Nuclear Proteins
  • Ubiquitin-Protein Ligases
  • seven in absentia proteins

Grants and funding

RSH is supported by the Stowers Institute for Medical Research and is an American Cancer SocietyResearch Professor. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.